Non-metric dental traits in great apeas

Varsha C Pilbrow

Leakey final report, June 2014

Leakey Foundation Final Report Non-metric dental traits in great apes Varsha C Pilbrow1 and Shara Bailey2 1. University of Melbourne, Department of Anatomy and Neuroscience 2. New York University, Department of Anthropology Research summary The objectives of our research project are to describe non-metric dental traits in extant great apes, provide an understanding of the nature of interspecific and intraspecific variation in such traits, and develop a set of dental plaques showing the gradations in expression of traits. It is expected that the great ape dental trait system will be used widely in paleoanthropology alongside the Arizona State University Dental Anthropology System (ASUDAS), currently available for humans. Together they will provide an objective and easily replicable dental scoring system. This comprehensive system will have potential for studying the homology of dental traits, for characterizing the nature of dental variation in fossil hominids, and for providing an understanding of the taxonomy and phylogeny of fossil and extant hominids. While the research project, as written, would have had us visiting South Africa, applying our newly devised dental trait system to re-assess the taxonomy of Paranthropus and Australopithecus, this goal had to be abandoned as our grant award was reduced from the proposed budget.

Nonetheless, we were able to achieve our objectives and we will soon have a great ape dental scoring system that promises to have wide applicability.

Progress to date Our progress is best described by reviewing the stages of the project: getting together to finalize the trait list and scoring categories, visiting museums in Europe and the USA to make dental casts of representative teeth, describing patterns of variation and presenting summaries of these results to scientific audiences, and making distribution quality dental plaques showing grades for each trait.

Finalizing the trait list: In putting together a list of dental traits and scoring categories we relied on our individual research expertise: Bailey’s on modern humans, the ASUDAS and fossil hominins, mine on modern apes and Miocene hominids. An early realization was that the background literature on dental morphology and non-metric dental traits is far more extensive for modern humans than it is for great apes. The ASUDAS scoring procedures developed by Turner et al. (1991) mark the culmination of several decades of research describing dental morphology and documenting patterns of variation in worldwide human populations (for example, HrdliÄ?ka, 1920; Campbell, 1925; Dahlberg, 1945, 1950, 1965; Korenhof, 1960; Hanihara, 1966). This information was readily accessible and formed the basis of fossil hominin dental morphological descriptions (Robinson, 1956; Sperber, 1974), although it was clear that the modern human morphology did not capture the morphological details seen in the fossils (Wood et al., 1983; Wood & Abbott, 1983; Wood & Uytterschaut, 1987; Wood and Englemann, 1988; Van Reenan & Reid, 1995; Schwartz et al., 1998). In contrast, very few researchers have described dental morphological details in apes, or provided scoring standards (Schuman and Brace, 1955; Remane, 1960, 1965; Frisch, 1965; Swindler, 1976).

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Varsha C Pilbrow

Leakey final report, June 2014

Furthermore, the terms and trait descriptions for apes are based on the mammalian dental literature and differ significantly from that used for modern humans, which have arisen within the clinical dental context without recourse to the comparative literature.

When putting together a trait list for great apes we made note of traits that were similar in size, shape and placement in humans, but for which the terminology differed.

Examples include the tuberculum dentale on the upper central incisor in humans, known as the median lingual pillar in apes, carabelli’s cusp on the upper first molar in humans, called the pericone in apes, and the metaconule on the upper molars, which in humans may also be referred to as the fifth cusp (C5) and is found at the distal margin of the occlusal basin, but in apes is described as a cusp on the midline of the crista obliqua, thus is in the centre of the occlusal basin (Figure 1). In order that the human and ape dental systems are eventually integrated into a single system, we marked traits such as these for further studies of trait homology.

Figure 1. Comparison of traits in modern humans and paes. First two teeth are modern, the next three are ape

We finalized the trait list relying heavily on my previously developed list. We scored the traits on casts from the Daris Swindler collection, housed in the Bailey lab at New York University. We also scored traits and trialed our molding and casting technique with great apes specimens from the American Museum of Natural History, New York. We then completed an inter-observer error study, each of us independently scoring the same specimens. This allowed us to identify traits that had high and low reliability in scoring and we altered our scoring categories and trait descriptions accordingly.

Visiting museums to make dental casts: I visited the following museums and made casts of representative dental traits: Museum American Museum of Natural History Natural History Museum, London Powell Cotton Museum University of Zurich Zoological State Collections, Munich Zoological Collections, Berlin Central African Museum, Tervuren Total

Gorilla 1 5 1 4

Pan 2

11 11 33

6 19 35

7 1

Pongo 1 3 26 3 33

Table 1. Museums visited and number of specimens studied at each

When choosing representative specimens for casting I took care that the teeth were unworn and provided good examples of the variable grades for the trait. I used a single trait list for all three great apes, but wasn’t able to find all trait categories in the

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Varsha C Pilbrow

Leakey final report, June 2014

specimens I studied. Bailey made an attempt to fill in the gaps and developed molds for 25 traits in Pan from the Museum of Comparative Zoology at Harvard University.

Presenting results to scientific audiences So far I have presented two papers on non-metric dental traits in great apes at the annual meetings of the American Association of Physical Anthropologists. “Discrete dental traits in chimpanzees” (American Journal of Physical Anthropology, Supplement 54:237) was presented in 2012. This research shows that chimpanzee species (Table 2) and subspecies of Pan troglodytes (Table 3) can be clearly differentiated by the frequency of occurrence of discrete dental traits.

Dental trait UI1 median lingual pillar LI1 median lingual pillar LI2 median lingual pillar LI1 mesial fovea LI2 mesial fovea UP3 distolingual tubercle UM2 anterior transverse crest LM2 tuberculum sextum (C6)

Pan paniscus 0% 37% 43% 0% 0% 74% 43% 2%

Pan troglodytes 54% 73% 81% 40% 47% 41% 83% 34%

Table 2. Dental trait differences between species of Pan. Chi-square probability <0.05

Dental trait UP4 mesiobuccal tubercle UP4 distobuccal tubercle LC distal groove UM2 protoconule UM3 protoconule UM3 distoconule LM1 trigonid crest LM3 trigonid crest LM3 tuberculum sextum (C6)

P. t. schweinfurthii 48% 82% 80% 66% 45% 62% 45% 65% 47%

P. t. troglodytes 13% 46% 53% 33% 20% 56% 24% 44% 55%

P. t. verus 7% 43% 56% 62% 36% 31% 70% 78% 28%

Table 3. Dental trait differences between subpecies of Pan troglodytes. Chi-square probability <0.05

A paper on gorilla dental trait variation, “Discrete dental traits differentiating Gorilla sexes, subspecies and species” (American Journal of Physical Anthropology 153 S58: 207) was presented to the same meetings in 2014 as a poster. The eastern and western species of Gorilla and the subspecies of each were distinguishable statistically by the frequency of occurrence of discrete dental traits; however, there was also a correlation between dental size and occurrence of dental traits, such that the dentally larger taxa had greater complexity of dental traits and increased frequencies of accessory tubercles (Figures 2, 3, 4).

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Varsha C Pilbrow

Leakey final report, June 2014

100 90 80 70 60 50 40 30 20

G. beringei G. gorilla

10 0

Figure 2. Discrete dental traits differentiating Gorilla species (Chi-square prob. <0.05)

100 90 80 70

60 50 40 30

G. g. gorilla

20

G. g. diehli

10 0

Figure 3. Discrete dental traits differentiating Gorilla gorilla sub-species (Chi-square prob. <0.05)

At present I am writing up these papers for publication. I am also working on presenting the results from a study of dental trait variation in Pongo for presentation at the scientific meetings. In addition, my collaborator, Bailey and I are undertaking a study on inter-observer error and inter-trait correlation with the aim of developing a list of traits to develop into plaques.

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Varsha C Pilbrow

Leakey final report, June 2014

Making distribution quality dental plaques While at the museums we took impressions of teeth and developed molds that captured the relevant dental traits. I used polyvinyl siloxane (PVS) molding material, but Bailey used soft putty impression material. These differences in materials ultimately affected the success of making casts from these molds. Upon returning from the museums we made first generation epoxy resin casts in our respective laboratories. I found the PVS molding material to be extremely pliable and was able to release the resin casts without undue damage to the molds. Bailey, however, did not have as much success with soft putty impression molds and split several molds when attempting to release the casts.

Fortunately, as the majority of the casts are being made from the PVS molds I developed, this has not proved to be a major setback in accomplishing the goals of the project.

100 90 80 70 60 50 40 30 20 10 0

G. b. graueri G. b. beringei

Figure 4. Discrete dental traits differentiating Gorilla beringei sub-species (Chi-square prob. <0.05)

When developing the project we had envisaged making replicas of grades of expression of each trait and mounting these on Plexiglas with the trait name and grade of expression labelled using an embossing label maker. These would be the master plaques. From these we were to generate silicone rubber master molds. We had planned to use gypsum dental stone (also known as Caststone) with high compressive strength to produce sets of plaques for distribution. However, with advances in threedimensional (3D) scanning and printing in the last couple of years we were able to accomplish the steps of making the base plaque and mounting teeth onto them digitally.

We scan the tooth with the trait in question using a 0.03 mm resolution Solutionix DS2 laser scanner. We use Geomagic Studio to isolate the tooth displaying the trait and use Meshlab to make a digital base. Using Geomagic Studio and Meshlab we then place each tooth on the digital plaque at set intervals and use embossed writing to name the plaque and note the grades of expression for the trait. The digital 3D plaque can then be printed using a high-resolution 3D printer. We trialed this method and printed the plaque showing gradations in the expression of the LP3 metaconid (Figure 5). The 3D laser scanner is housed in my lab and 3D laser printers are available at the University of Melbourne. This stage of the project will therefore be completed in my lab in Australia.

Three dimensional printing is quite affordable at $25-30 per plaque, and will save considerable time and effort over making older style plaster plaques.

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Varsha C Pilbrow

Leakey final report, June 2014

Figure 5. Photograph of a dental plaque developed by 3D laser scanning and 3D printing Continuing work We are continuing to work on several parts of this project simultaneously to see it to fruition. I am writing papers on patterns of non-metric dental trait variation in great apes, completing the casting project and developing casts of teeth for laser scanning. I will then review each trait and trait expression in great apes and humans and develop a list of traits that are common to both groups, and another list that is unique to each group. With my collaborator Bailey I will work on inter-observer error and inter-trait correlation studies so as to finalize a list of highly reliable traits for developing into plaques for distribution.

Publications In addition to the abstracts published in the American Journal of Physical Anthropology (Pilbrow, 2012, 2014), we plan the following publications: Dental traits in chimpanzees Dental size and non-metric trait complexity in gorillas Dental trait variation in orangutans Inter-trait correlation and inter-observer error in non-metric dental traits in extant great apes Future work Future work will look at traits that are common to the great ape and human groups but differ in their expression. We will study such traits below the level of the enamel at the enamel-dentine junction to establish the precursor morphology and phylogenetic continuity in these traits. Once a dental trait system for great apes is established I will use this to study dental morphological variation in Paranthropus and Australopithecus in South Africa. Although the Leakey grant did not permit us to do that part of the project, I was able to secure funds from the department of Anatomy and Neuroscience at the University of Melbourne that will allow me to travel to South Africa to test the applicability of the new system. We acknowledge that the great ape dental scoring system is preliminary at this stage and that further work will help to strengthen it. I will be applying for further funding to document the frequency of the traits in populations of great apes, so as to provide a comparative database for future studies.

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References:

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Dahlberg, A. A. (1965). Geographic distribution and origin of dentitions. Intl. Dent. J. 15, 42-49.

Frisch, J. E. (1965) Trends in the Evolution of the Hominoid Dentition. In Bibliotheca Primatologica. H. Hoffer, A. H. Schultz, and D. Starck, eds. Vol. 3. Basel:Karger.

Hanihara, K. (1966). Mongoloid dental complex in the deciduous dentition. J. Anthropol. Soc. Jap 74, 61–72.

Hrdlička A. 1920. Shovel-shaped teeth. Am J Phys Anthropol 3:429–465.

Korenhof, C. A. W. (1960) Morphogenetical Aspects of the Human Upper Molar.

Uitgeversmaatschappij Neerlandia: Utrecht.

Pilbrow, VC. (2014). Discrete dental traits differentiating Gorilla sexes, subspecies and species.

American Journal of Physical Anthropology 153 S58:207.

Pilbrow, VC. (2012). Discrete dental traits in chimpanzees. American Journal of Physical Anthropology. Supplement 54:237.

Remane, A. (1960) Zähne und Gebiss.Primatologica, III: 637-846.

Remane, A. (1965) Die Geschichte der Menschenaffen. In Menschliche Abstammungslehre. Pp. 249-309. Stuttgart: Gustav Fischer.

Robinson, J.T., (1956). The Dentition of the Australopithecinae. Transvaal Museum Memoir No. 9.

Schuman, E., and C. L. Brace (1955) Metric and Morphological Variations in the Dentition of the Liberian Chimpanzee: Comparison with Anthropoid and Human Dentitions. In The Nonhuman Primates and Human Evolution. J. Gavan, ed. Pp. 61-90. Detroit: Wayne State University Press.

Schwartz, G., Thackeray, F., Reid, C. & van Reenan, J. F., (1998). Enamel thickness and the topography of the enamel–dentine junction in South African Plio-Pleistocene hominids with special reference to the Carabelli trait. J. Hum. Evol. 35(4-5), 523–542.

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Turner, C. G. II, Nichol, C. R. & Scott, G. R. (1991). Scoring procedures for key morphological traits of the permanent dentition: the Arizona State University dental anthropology system.

In Kelley, M. A. & Larsen, C. S. (Eds.) Advances in Dental Anthropology (pp. 13-31). New York: Wiley-Liss.

Van Reenan, J. & Reid, C. (1995). The Carabelli trait in early South African hominids: a morphometrics study. In Moggi-Cecchi, J (Ed), Aspects of Dental Biology: Paleontology, Anthropology and Evolution (pp. 299–304). Florence: International Institute for the Study of Man. Wood, B. A., & Abbott, S. A. (1983a). Analysis of the dental morphology of Plio-Pleistocene hominids. I. Mandibular molars: crown area measurements and morphological traits. J. Anat.

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Wood, B. A., Abbott, S. A. & Graham, S. H. (1983b). Analysis of the dental morphology of PlioPleistocene hominids. II. Mandibular molars: study of cusp areas, fissure pattern and cross sectional shape of the crown. J. Anat. 137, 287–314.

Wood, B. A. & Uytterschaut, H. (1987). Analysis of the dental morphology of Plio-Pleistocene hominids. III. Mandibular premolar crowns. J. Anat. 154, 121-156.

Wood B. A., & Engleman, C.A. (1988). Analysis of the dental morphology of Plio-Pleistocene hominids. V. Maxillary postcanine tooth morphology. J. Anat. 161, 1-35.

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